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Long noncoding RNAs (lncRNAs) have emerged as diverse functional regulators involved in mammalian development; however, large-scale functional investigation of lncRNAs in mammalian spermatogenesis in vivo is lacking. Here, we delineated the global lncRNA expression landscape in mouse spermatogenesis and identified 968 germ cell signature lncRNAs. By combining bioinformatics and functional screening, we identified three functional lncRNAs ( Gm4665 ,  1700027A15Rik , and  1700052I22Rik ) that directly influence spermatogenesis in vivo. Knocking down  Gm4665  hampered the development of round spermatids into elongating spermatids and disrupted key spermatogenic gene expression. Mechanistically, lncRNA  Gm4665  localized in the nucleus of round spermatids and occupied the genomic regulatory region of important spermatogenic genes including  Ip6k1  and  Akap3 . These findings provide a valuable resource and framework for future functional analysis of lncRNAs in spermatogenesis and their potential roles in other biological processes.

Panoramic transcriptome analysis and functional screening of long noncoding RNAs in mouse spermatogenesis